Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in wild birds

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1785, 2014, Pages

  Boonekamp, Jelle J ^a   Mulder, G A ^a   Salomons, H Martijn ^a   Dijkstra, Cor ^a   Verhulst, Simon ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Ageing; Biomarker; Growth; Jackdaw

Indexed keywords

AGING POPULATION; BIOMARKER; BIRD; BROOD SIZE; DEVELOPMENTAL BIOLOGY; FITNESS; FLEDGING; GROWTH RATE; MORTALITY; NESTLING; PREDICTION; RECRUITMENT (POPULATION DYNAMICS); SURVIVAL; WILD POPULATION;

ANIMAL; ANIMAL EMBRYO; ANURA; EMBRYOLOGY; MALE; MEXICO; PATERNAL BEHAVIOR; PHYSIOLOGY; REPRODUCTION;

ANIMALS; ANURA; EMBRYO, NONMAMMALIAN; EMBRYOLOGY; MALE; MEXICO; PATERNAL BEHAVIOR; PHYSIOLOGY; REPRODUCTION;

EID: 84899680527     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.3287     Document Type: Article

References (43)

1. Lindström J. 1999 Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343-348. (doi:10.1016/S0169-5347(99)01639-0)
2. Lummaa V, Clutton-Brock T. 2002 Early development, survival and reproduction in humans. Trends Ecol. Evol. 17, 141-147. (doi:10.1016/ S0169-5347(01)02414-4)
3. Armanios M, Blackburn EH. 2012 The telomere syndromes. Nat. Rev. Genet. 13, 693-704. (doi:10. 1038/nrg3246)
4. Olovnikov AM. 1973 A theory of marginotomy: the incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41, 181-190. (doi:10.1016/0022-5193(73) 90198-7)
5. Stewart S, Ben-Porath I, Carey V, O'Connor BF, Hahn WC, Weinberg RA. 2003 Erosion of the telomeric single-strand overhang at replicative senescence. Nat. Genet. 33, 492-496. (doi:10.1038/ng1127)
6. Zglinicki von T. 2002 Oxidative stress shortens telomeres. Trends Biochem. Sci. 27, 339-344. (doi:10.1016/S0968-0004(02)02110-2)
7. Joeng KS, Song EJ, Lee K-J, Lee J. 2004 Long lifespan in worms with long telomeric DNA. Nat. Genet. 36, 607-611. (doi:10.1038/ng1356)
8. Haussmann MF, Winkler D, Vleck CM. 2005 Longer telomeres associated with higher survival in birds. Biol. Lett. 1, 212-214. (doi:10.1098/rsbl. 2005.0301)
9. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P. 2009 Telomere dynamics rather than age predict life expectancy in the wild. Proc. R. Soc. B 276, 1679-1683. (doi:10.1098/rspb.2008.1817)
10. Salomons HM, Mulder E, van de Zande L, Haussmann MF, Linskens M, Verhulst S. 2009 Telomere shortening and survival in free-living corvids. Proc. R. Soc. B 276, 3157-3165. (doi:10. 1098/rspb.2009.0517)
11. Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P. 2012 Telomere length in early life predicts lifespan. Proc. Natl Acad. Sci. USA 109, 1743-1748. (doi:10.1073/pnas.1113306109)
12. Angelier F, Vleck CM, Holberton RL, Marra PP. 2013 Telomere length, non-breeding habitat and return rate in male American redstarts. Funct. Ecol. 27, 342-350. (doi:10.1111/1365-2435.12041)
13. Barrett EL, Burke TA, Hammers M, Komdeur J, Richardson DS. 2013 Telomere length and dynamics predict mortality in a wild longitudinal study. Mol. Ecol. 22, 249-259. (doi:10.1111/mec.12110)
14. Boonekamp JJ, Simons MJP, Hemerik L, Verhulst S. 2013 Telomere length behaves as biomarker of somatic redundancy rather than biological age. Aging Cell 12, 330-332. (doi:10.1111/acel.12050)
15. Caprioli M, Romano M, Romano A, Rubolini D, Motta R, Folini M, Saino N. 2013 Nestling telomere length does not predict longevity, but covaries with adult body size in wild barn swallows. Biol. Lett. 9, 20130340. (doi:10.1098/rsbl.2013.0340)
16. Monaghan PP, Haussmann MFM. 2005 Do telomere dynamics link lifestyle and lifespan? Trends Ecol. Evol. 21, 47-53. (doi:10.1016/j.tree.2005.11.007)
17. Bakaysa SL, Mucci LA, Slagboom PE, Boomsma DI, McClearn GE, Johansson B, Pedersen NL. 2007 Telomere length predicts survival independent of genetic influences. Aging Cell 6, 769-774. (doi:10. 1111/j.1474-9726.2007.00340.x)
18. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM. 2004 Accelerated telomere shortening in response to life stress. Proc. Natl Acad. Sci. USA 101, 17 312-17 315. (doi:10. 1073/pnas.0407162101)
19. Pauliny AA, Larsson KK, Blomqvist DD. 2011 Telomere dynamics in a long-lived bird, the barnacle goose. BMC Evol. Biol. 12, 257. (doi:10. 1186/1471-2148-12-257)
20. Frenck RW, Blackburn EH, Shannon KM. 1998 The rate of telomere sequence loss in human leukocytes varies with age. Proc. Natl Acad. Sci. USA 95, 5607-5610. (doi:10.1073/pnas.95.10.5607)
21. Rufer N, Brümmendorf TH, Kolvraa S, Bischoff C, Christensen K, Wadsworth L, Schulzer M, Lansdorp PM. 1999 Telomere fluorescence measurements in granulocytes and T lymphocyte subsets point to a high turnover of hematopoietic stem cells and memory T cells in early childhood. J. Exp. Med. 190, 157-167. (doi:10.1084/jem.190.2.157)
22. Zeichner SLS, Palumbo PP, Feng YY, Xiao XX, Gee DD, Sleasman JJ, Goodenow MM, Biggar RR, Dimitrov DD. 1999 Rapid telomere shortening in children. Blood 93, 2824-2830.
23. Entringer S, Epel ES, Kumsta R, Lin J, Hellhammer DH, Blackburn EH, Wüst S, Wadhwa PD. 2011 Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood. Proc. Natl Acad. Sci. USA 108, E513-E518. (doi:10.1073/ pnas.1107759108)
24. Haussmann MFM, Longenecker ASA, Marchetto NMN, Juliano SAS, Bowden RMR. 2012 Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc. R. Soc. B 279, 1447-1456. (doi:10. 1098/rspb.2011.1913)
25. Geiger S, le Vaillant M, Lebard T, Reichert S, Stier A, Maho YL, Criscuolo F. 2012 Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol. Ecol. 21, 1500-1510. (doi:10.1111/j.1365-294X.2011.05331.x)
26. Hall ME, Nasir L, Daunt F, Gault EA, Croxall JP, Wanless S, Monaghan P. 2004 Telomere loss in relation to age and early environment in long-lived birds. Proc. R. Soc. Lond. B 271, 1571-1576. (doi:10.1098/rspb.2004.2768)
27. Voillemot M, Hine K, Zahn S, Criscuolo FO, Gustafsson L, Doligez B, Bize P. 2012 Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecol. 12, 1-8. (doi:10.1186/1472-6785-12-17)
28. Nettle D, Monaghan P, Boner W, Gillespie R, Bateson M. 2013 Bottom of the heap: having heavier competitors accelerates early-life telomere loss in the European starling, Sturnus vulgaris. PLoS ONE 8, e83617. (doi:10.1371/journal.pone.0083617)
29. Salomons HM, Dijkstra C, Verhulst S. 2008 Strong but variable associations between social dominance and clutch sex ratio in a colonial corvid. Behav. Ecol. 19, 417-424. (doi:10.1093/beheco/arm149)
30. Perrins CM. 1965 Population fluctuations and clutch-size in the great tit, Parus major L. J. Anim. Ecol. 34, 601-647. (doi:10.2307/2453)
31. Verhulst S, Salomons HM. 2004 Why fight? Socially dominant jackdaws, Corvus monedula, have low fitness. Anim. Behav. 68, 777-783. (doi:10.1016/j. anbehav.2003.12.020)
32. Naguib M, Riebel K, Marzal A, Gil D. 2004 Nestling immunocompetence and testosterone covary with brood size in a songbird. Proc. R. Soc. Lond. B 271, 833-838. (doi:10.1098/rspb.2003.2673)
33. Verhulst S, Holveck M-J, Riebel K. 2006 Long-term effects of manipulated natal brood size on metabolic rate in zebra finches. Biol. Lett. 2, 478-480. (doi:10.1098/rsbl.2006.0496)
34. Metcalfe NB, Monaghan P. 2001 Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16, 254-260. (doi:10.1016/S0169-5347(01)02124-3)
35. Bauch C, Becker PH, Verhulst S. 2014 Within the genome, long telomeres are more informative than short telomeres with respect to fitness components in a long-lived seabird. Mol. Ecol. 23, 300-310. (doi:10.1111/mec.12602)
36. Foote CG, Daunt F, González-Solís J, Nasir L, Phillips RA, Monaghan P. 2011 Individual state and survival prospects: age, sex, and telomere length in a longlived seabird. Behav. Ecol. 22, 156-161. (doi:10. 1093/beheco/arq178)
37. Broer L et al. 2013 Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur. J. Hum. Genet. 21, 1163-1168. (doi:10.1038/ ejhg.2012.303)
38. Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz T, Blomqvist D. 2011 Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLoS ONE 6, e17473. (doi:10.1371/journal. pone.0017473)
39. Horn T, Robertson BC, Will M, Eason DK, Elliott GP, Gemmell NJ. 2011 Inheritance of telomere length in a bird. PLoS ONE 6, e17199. (doi:10.1371/journal. pone.0017199)
40. Verhulst S, Aviv A, Benetos A, Berenson GS, Kark JD. 2013 Do leukocyte telomere length dynamics depend on baseline telomere length? An analysis that corrects for 'regression to the mean'. Eur. J. Epidemiol. 28, 859-866. (10.1007/s10654-013-9845-4)
41. Batista LFZ et al. 2011 Telomere shortening and loss of self-renewal in Dyskeratosis congenita induced pluripotent stem cells. Nature 474, 399-402. (doi:10.1038/nature10084)
42. Choudhury AR et al. 2006 Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation. Nat. Genet. 39, 99-105. (doi:10.1038/ ng1937)
43. Capper R, Britt-Compton B, Tankimanova M, Rowson J, Letsolo B, Man S, Haughton M, Baird DM. 2007 The nature of telomere fusion and a definition of the critical telomere length in human cells. Genes Dev. 21, 2495-2508. (doi:10.1101/gad.439107)